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Somatosensory evoked potentials: Abnormalities with focal brain lesions remote from the primary sensorimotor area
Electroencephalography and Clinical Neurophysiology, 1980, 49:59--65
59
© Elsevier/North-Holland Scientific Publishers, Ltd.
S O M A T O S E N S O R Y E V O K E D POTENTIALS: A B N O R M A L I T I E S WITH FOCAL BRAIN LESIONS REMOTE F R O M THE P R I M A R Y S E N S O R I M O T O R A R E A 1 J.A. OBESO, J.F. MARTI-MASSO and N. CARRERA Division of Neurology, Residencia Sanitaria Nuestra Sra. de Aranzazu, San Sebastian (Spain)
(Accepted for publication: September 13, 1979) The clinical applications of somatosensory evoked potentials (SEPs) by means of an averaging technique have been extensively reported (Halliday 1967; Laget et al. 1967; Williamson et al. 1970; Desmedt and Noel 1973; Cracco 1975). Most previous studies have associated clinical impairment of joint position sensitivity with the appearance of SEP abnormalities (Halliday and Wakefield 1963; Giblin 1964; Noel and Desmedt 1975). Thus the integrity of both the dorsal columnmedial lemniscus pathway and primary sensorimotor area (PSMA) has been considered an essential requirement to record a normal SEP (Domino et al. 1965; Stohr and Goldring 1969). On the contrary, isolated lesions of the dorso-lateral ascending pathways or those placed away from the PSMA did n o t modify SEP characteristics (Bergamini and Bergamasco 1967; Halliday 1967; Noel and Desm e d t 1975). However, there are suggestions that SEPs contain several components arising from different neuronal sources, the early short latency potentials corresponding to the lemniscus-mediated responses and the late waves to the diffuse spino-thalamic projections (Abrahamian et al. 1963; Shagass and Schwartz 1964; Lewis 1970; Yamada et al. 1977). Recent investigations have shown altered SEPs in patients w i t h o u t sensory disturbances (Okasaki et al. 1971; Shibasaki et al. 1977; Yamada et al. 1978), giving a new dimension to the role of SEPs in assessing
brain activity under pathological conditions. The present work analyses the influence on SEPs of focal brain lesions placed remote from the PSMA, using the high accuracy of computerized tomography in detecting and localizing brain lesions (Ambrose et al. 1975; Jabobs et al. 1976).
Methods and materials Subjects
A total of 41 patients with supratentorial focal brain lesions was studied, 14 cases of brain t u m o r and 27 of cerebrovascular accident (Table I). Their ages ranged between 22 and 72 years. An equal number of normal volunteers served as controls. The site of the pathological lesion was determined in all cases by computerized tomography (CT). Clinical examination was performed by at least two neurologists on different days. Special care was taken to avoid the influence of acute changes in the clinical situation; thus no patient with cerebrovascular accident (CVA) was explored during the acute phase of the illness (first 2 weeks). To facilitate statistical analysis, subjects were arranged in 3 groups: group I, patients with lesions of the PSMA; group II, patients with lesions remote from the PSMA; and group III, normal volunteers (Table I). Clinical data
i Presented in part at the International Evoked Potentials Symposium, Nottingham (U.K.), 1978.
Sensory impairment as judged clinically was present in all patients of group I. 80% had
60
sensory deficits for all modalities, 11% presented mainly pain and temperature loss, and 18% showed visual agnosia, anosognosia and asomatognosia. In group II, 5 patients (24%) were f o u n d to have sensory defects, 3 were cases of tactile extinction and 2 of agraphaesthesia.
Recording procedure A Medelec electrophysiological system was used. SEPs were recorded in a dimly lit shielded room with the subject in a supine position with the eyes closed. The median nerve was electrically stimulated at the wrist, using a pair of surface electrodes placed 3 cm apart. Pulse duration was 0.1 msec. The stimulus intensity was adjusted to 10% above the m o t o r threshold of the opponens pollicis muscle in each case. Stimuli were delivered at intervals of 1--2 sec. Insulated stainless steel needles with a bared tip of 5 m m were used for recording both EEGs and SEPs. To record the SEPs, the active electrode was placed on C3 or C4 (10-20 system), and the reference electrode on Fz. The amplifier bandpass was 10--2000 c/sec (--3 dB), and the outputs were s u m m a t e d by a computer (Plurimat-S). Polaroid films were used to make permanent records of all potentials. One set of tests consisted of 256 averaged responses with an analysis time of 200 msec. Latencies were measured from the stimulus to each peak with a resolution of 0.2 msec. Amplitudes were defined as the heights of successive positivenegative peaks. Two-way analysis of variance and ×2 test were used for statistical analysis.
J.A. O B E S O E T AL.
]5"
flTO 10 S 0 5
+%%
p.
%,~
10
(÷)
50
150
IO0
did n o t reach statistical significance ( P > 0.05).
Relationship o f SEP abnormalities to the site and aetiology o f the lesion SEP abnormalities were f o u n d on the same side as the lesion in 20 out of 21 patients from group I (90%) and in 15 patients (71%) from group II. Over the intact hemisphere SEPs were altered in 9 cases (43%) from group I, and in 3 patients (15%) from group II (Table I). The aetiology of the lesion was not a significant factor for the incidence of abnormalities in either group (×2 test, P > 0.05). TABLE I SEP a b n o r m a l i t i e s a n d sites o f t h e lesions a c c o r d i n g t o aetiology. Localization
Results
Tumours
CVA *
Control group (III) SEP values for this group were similar to those reported by other authors (Giblin 1964; Desmedt and Noel 1973; Shibasaki et al. 1977; Yamada et al. 1978). In Fig. 1 a schematic SEP is the model of normality considered in this work. Variability between hemispheres, both individual and within the group,
200
Fig. 1. S c h e m a t i c SEP b y m e d i a n n e r v e s t i m u l a t i o n , w h i c h r e p r e s e n t s t h e average o f 40 n o r m a l v o l u n t e e r s . Positive waves are d o w n w a r d , b y c o n v e n t i o n in this a n d s u b s e q u e n t figures. T i m e in msec, a m p l i t u d e in mV.
A b n o r m a l SEP Affected side
Intact side
Group I PSMA
4
17
19
9
7 1 2
4 5 1
10 3 2
2 0 1
Group H Frontal Occipital Temporal
* CVA = cerebrovascular accident.
SEP ABNORMALITIES WITH FOCAL BRAIN LESIONS
61
TABLE II SEP abnormalities in patients with focal brain lesions. J~, increased latency;-~, decreased amplitude; t, increased duration; t t , increased amplitude. Affected hemisphere
Intact hemisphere
N-22
N-39
N-70
N-22
N-39
N-70
~t
19 17 5 0
18 11 14 0
12 6 3 0
4 2 8 7
3 6 5 5
0 3 3 2
5
2
2
0
0
0
t t~
4 10 16
4 15 14
4 7 9
0 2 2
0 1 2
0 0 0
G r o u p I (n = 21)
Group II (n = 20)
Relationship o f clinical data to SEP alterations When e v e r y i s o l a t e d p a r a m e t e r o f SEP was a n a l y s e d (Table II), i n c r e a s e d l a t e n c y a n d d e p r e s s e d a m p l i t u d e o f t h e first t w o waves (N-22 a n d N - 3 9 ) c o r r e l a t e d significantly w i t h lesions o f t h e P S M A a n d w i t h s e n s o r y deficits, while r e m o t e lesions a p p e a r e d t o be assoc i a t e d with i n c r e a s e d a m p l i t u d e o f N-22 a n d N - 3 9 (×: test, P < 0.01). T h e i n c i d e n c e o f SEP a n o m a l i e s in t h e i n t a c t h e m i s p h e r e was g r e a t e r in g r o u p I t h a n in g r o u p I I (P < 0.01). N e v e r t h e l e s s , t h e c h a n g e s in m o r p h o l o g y in t h e s e cases were similar t o t h o s e seen w i t h r e m o t e lesions on t h e a f f e c t e d h e m i s p h e r e (Fig. 2, 3 a n d 4). A b n o r m a l i t i e s o f the N-70 w a v e were p r e s e n t e q u a l l y in t h e t w o g r o u p s (×2 test, P > 0.05).
EEG and SEP abnormalities
Fig. 2. Top: CT scan showing a large right hemisphere infarct. Bottom: SEP of the left hemisphere (upper) and of the right (lower). Note that SEP is almost absent on the affected side and also abnormal on the intact side.
A c o m p a r a t i v e analysis o f t h e discriminat o r y p o w e r s o f SEPs a n d E E G s f o r d e t e c t i n g b r a i n d y s f u n c t i o n s h o w e d a slight s u p e r i o r i t y o f SEPs in b o t h g r o u p s a n d o v e r b o t h h e m i s p h e r e s (Table I I I ) . T h e s e d i f f e r e n c e s were significant for group I on the intact hemisphere a n d f o r g r o u p I i on t h e a f f e c t e d side (P < 0.01).
62
J.A. OBESO ET AL.
Fig. 4. Top: CT scan of a patient with a left occipital haematoma. Bottom: abnormal SEP, waves N-22 and N-39, on the affected side (upper) and normal response on the intact hemisphere (lower).
Fig. 3. Top: extensive temporo-parietal infarction on the right and small frontal infarct on the left. Bottom: the SEP on the left (upper) represents a typical trace for patients with lesions remote from the PSMA; the early waves are increased in amplitude and period, while the SEP recorded on the right (lower) is almost absent.
a n d N-39 (Giblin 1 9 6 4 ; Liberson 1 9 6 6 ; Laget et al. 1 9 6 7 ; Halliday 1 9 6 7 ; T s u m o t o et al. 1 9 7 3 ; Shibasaki et al. 1 9 7 7 ; Y a m a d a et al. 1 9 7 8 ) . B o t h changes c o r r e l a t e d well with clinical s e n s o r y deficits, as in m a n y o t h e r r e p o r t s ( A l a j o u a n i n e et al. 1 9 5 8 ; Halliday a n d Wake-
TABLE III Comparison of SEP and EEG rates of abnormality. Discussion On c o n s i d e r i n g the r e l a t i o n s h i p b e t w e e n SEP a b n o r m a l i t i e s a n d lesions involving the PSMA, o u r s t u d y c o n f i r m s a n d f u r t h e r d o c u m e n t s previous findings r e p o r t i n g l o n g e r latencies and r e d u c t i o n in a m p l i t u d e o f N-22
Group I Group II
Affected hemisphere
Intact hemisphere
SEP
EEG
SEP
EEG
19 16
18 12
10 3
4 2
SEP ABNORMALITIES WITH FOCAL BRAIN LESIONS field 1963; Bergamini and Bergamasco 1967; Desmedt and Noel 1973). The high incidence of SEP abnormalities among patients with lesions placed far away from the PSMA represents the most important finding of this study. These anomalies reveal a brain dysfunction remote from the original lesion, since both clinical and experimental research have clearly shown that PSMA is the main source of the early SEP waves (Kelly et al. 1965; Velasco and Velasco 1975; Lukas and Siegel 1977; Goff et al. 1977; Iragui-Madoz and Wiederholt 1977). This concept is very close to Von Monakow's theory of diaschisis (1914), which was first invoked by Larson et al. (1966) to explain their finding of SEP abnormalities in the intact hemisphere of patients with unilateral lesions. Studies on brain glucose metabolism (Meyer et al. 1970), regional cerebral blood flow (Endo et al. 1977; Slater et al. 1977) and cortical electrophysiology (Kempinsky 1958) support Von Monakow's original theory. From a purely neurophysiological point of view, we may state that lesions destroying the PSMA elicit an increase in latency and a decrease in amplitude of c o m p o n e n t s N-22 and N-39, as shown in Figs. 2 and 3. On the other hand, the main changes f o u n d in group II are increased duration and amplitude of N-22 and N-39 (Figs. 3 and 4). The latter changes may be interpreted as due to neuronal hypersynchronism secondary to metabolic alterations of PSMA neurones (Creutzfeldt and Houchin 1974), although direct evidence is n o t available yet. Changes of N-70 and later waves did n o t prove to be specific in our patients as was previously recognized by other authors (Shibasaki et al. 1977; Yamada et al. 1978). The N-70 wave seems to be subject to reticular influences and, thus, to reflect more closely the functional state of the reticulocortical pathways (Lukas and Siegel 1977). As a whole, SEPs are only slightly superior to the EEG in their ability to detect abnormalities. However, SEPs are of considerably greater value in localizing brain dysfunction, in agreem e n t with earlier publications (Mijoshi et al.
63 1971; Shibasaki et al. 1977). Present results allow the use of SEPs as a functional test to evaluate patients with cerebral lesions of any origin. Moreover, these findings may be a starting point to study the cortical mechanism involved in the recovery of certain brain functions after focal lesions, a matter of practical and theoretical interest.
Summary Somatosensory evoked potentials (SEPs) were recorded in 41 patients with focal brain lesions recognized by computerized tomography. 21 patients presented damage of the primary sensorimotor area (PSMA), and their SEPs were reduced in amplitude and increased in latency for the t w o early components (N-22 and N-39), in accordance with previous evidence. The other 20 patients presented lesions remote from the PSMA, 15 (71%) showing abnormal SEPs mainly c'haracterized by increment in amplitude and duration of N-22 and N-39. Abnormalities of the N-70 and later waves were n o t specific for any type of lesion. SEPs appeared more sensitive than the EEG for detecting brain dysfunction. The physiopathological and clinical importance of these findings are discussed.
Rdsumd Potentiels dvoquds somesthdsiques: anomalies rdsultant de ldsions focales du cortex sensorimoteur Les potentiels ~voqu~s somesth~siques (PES) ont dtd etudids chez 41 malades atteints de ldsions c~r~brales focales confirmdes par tomodensitomdtrie (TAC). Une ldsion du cortex sensorimoteur primaire (CSMP) a ~t~ d~celde chez 21 malades; leurs PES dtaient caractdrisds par une augmentation de la latence et une diminution de l'amplitude des premieres composantes (N-22, N-39). Les 20 autres malades, porteurs d'altdrations dioign~es du
64 CSMP, ont pr~sent~ une augmentation de l'amplitude et de la dur~e de N-22 et de N-39. Les anomalies de N-70 et des ondes plus tard i v e s n ' o n t ~t~ e n c o r r e l a t i o n a v e c a u c u n type de l~sion. Les PES semblent ainsi ~tre plus sensibles que I'EEG, pour la d~tection des l~sions c~r~brales. Les auteurs discutent l'importance physiopathologique et clinique de ces donn~es. References Abrahamian, H.A., Allison, T., Goff, W.R. and Rosnet, B.S. Effects of thiopenthai on human cerebral evoked responses. " Anesthesiology, 1963, 24: 650---657. Alajouanine, Th., Scherrer, J., Barbizet, J., Calvet, J. et Verley, R. Potentiels ~voqu~s corticaux chez des sujets atteints des troubles somesth~siques. Rev. neurol., 1958, 98: 757--762. Ambrose, J., Gooding, M.R. and Richardson, A.E. An assessment of the accuracy of computerized axial scanning in the diagnosis of intracranial tumors. A review of 366 patients. Brain, 1975, 98:. 559--582. Bergamini, L. and Bergamasco, B. Possibility of the clinical use of sensory evoked potentials transcranially recorded in man. In: W. Cobb and C. Morocutti (Eds.), The Evoked Potentials. Electroenceph. clin. Neurophysiol., 1967, Suppl. 26: 114--122. Cracco, R.Q. Clinical applications of averaged evoked responses to somatic stimulation. Int. J. Neurol., 1975, 9: 233--246. Creutzfeldt, O. and Houchin, J. Neuronal basis of EEG waves. In: A. R~mond (Ed.), Handbook of Electroenceph. clin. Neurophysiol., Vol. 2. Elsevier, Amsterdam, 1974: 5--54. Desmedt, J.E. and Noel, P. Average cerebral evoked potentials in the evaluation of lesions of the sensory nerves and of the central somatosensory pathway. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 2. Karger, Basel, 1973: 352--371. Domino, E.F., Matsuoka, S., Waltz, J. and Cooper, I.J. Effects of cryogenic thalamic lesions on the somesthesic evoked response in man. Electroenceph. clin. Neurophysiol., 1965, 19: 127--138. Endo, H. and Larsen, B. Regional cerebral blood flow alterations remote from the site of intracranial tumors. J. Neurosurg., 1977, 40: 271--281. Giblin, D.R. Somatosensory evoked potentials in healthy subjects and in patients with lesions of the nervous system. Ann. N.Y. Acad. Sci., 1964, 223: 93--141.
J.A. OBESO ET AL. Goff, G.D., Matsumiya, Y., Allison, T. and Goff, W.R. The scalp topography of human somatosensory and auditory evoked potentials. Electroenceph. clin. Neurophysiol., 1977, 42: 57--76. Halliday, A.M. Changes in the form of cerebral evoked responses in man associated with various lesions of the nervous system. Electroenceph. clin. Neurophysiol., 1967, Suppl. 25: 178--192. Halliday, A.M. and Wakefield, G.S. Cerebral evoked potentials in patients with dissociated sensory loss. J. Neurol. Neurosurg. Psychiat., 1963, 26: 211--219. HCedt-Rusmussen, K. and Skinh~by, E. Transmural depression of the cerebral hemispheric metabolism in man. Acta neurol, scand., 1964, 40: 41--46. Iragui-Madoz, V.J. and Wiederholt, W.C. Far-field somatosensory evoked potentials in the cat: correlation with depth-recording. Ann. Neurol., 1977, 1 : 569--574. Jacobs, L., Kankel, W.R. and Heffner, R. Autopsy correlations of computerized tomography: Experience with 6000 CT scans. Neurology (Minneap.), 1976, 26: 1111--1118. Kelly, D.S., Goldring, S. and O'Leary, J.L. Averaged evoked somatosensory responses from exposed cortex of man. Arch. Neurol. (Chic.), 1965, 13: 1--9. Kempinsky, W.A. Experimental study of distant effects of acute focal brain injury: a study of diaschisis. Arch. Neurol. Psychiat., 1958, 79: 376--389. Laget, P., Mamo, H. et Houdart, R. De l'int~r~t des potentiels ~voqu~s somesth~siques dans l'~tude des l~sions du lobe parietal de l'homme. Etude pr~liminaire. Neurochirurgie, 1967, 13: 841--853. Larson, S.J., Sances, A. and Christensen, P.C. Evoked somatosensory potentials in man. Arch. Neurol. (Chic.), 1966, 15: 88--93. Lewis, E.G. The effect of alcohol on visual and somatosensory evoked responses. Electroenceph. clin. Neurophysiol., 1970, 28: 202--205. Liberson, W.T. Study of evoked potentials in aphasics. Amer. J. phys. Med., 1966, 45: 135--142. Lukas, J.H. and Siegel, J. Cortical mechanisms that augment or reduce evoked potentials in cats. Science, 1977, 198: 73--75. Meyer, J.S., Shinohara, Y. and Konda, P. Diaschisis resulting from acute unilateral cerebral infarction. Arch. Neurol. (Chic.), 1970, 23: 241--247. Mijoshi, S., Luders, H., Kato, M. and Kuroiwa, Y. The somatosensory evoked potentials in patients with cerebrovascular diseases. Folia psychiat, neurol. jap., 1971, 25: 9--25. Nakanishi, T., Shimada, Y., Sakuta, M. and Toyokura, Y. The initial positive component of the scalp-recorded somatosensory evoked potential in normal subjects and in patients with neurological
SEP ABNORMALITIES WITH FOCAL BRAIN LESIONS disorders. Electroenceph. clin. Neurophysiol., 1978, 45: 26--34. Namerow, N.S. Somatosensory evoked responses in multiple sclerosis patients with varying sensory loss. Neurology (Minneap.), 1968, 18: 1197--1204. Noel, P. and Desmedt, J.E. Somatosensory evoked potentials after vascular lesions of the brain-stem and diencephalon. Brain, 1975, 98: 113--128. Okasaki, A., Shiota, T. and Terada, C. Clinical studies on the somatosensory evoked response in neurosurgical patients. Electroenceph. clin. Neurophysioi., 1971, 31: 189. Shagass, Ch. and Schwartz, M. Recovery function of somatosensory peripheral nerve and cerebral evoked responses in man. Electroenceph. clin. Neurophysiol., 1964, 17: 126--135. Shibasaki, H., Yamashita, Y. and Tsuji, S. Somatosensory evoked potentials. Diagnostic criteria and abnormalities in cerebral lesions. J. neurol. Sci., 1977, 34: 427--439. Slater, R., Reivich, M., Golberg, H., Bonka, R. and Greenberg, J. Diaschisis with cerebral infarction. Stroke, 1977, 8: 684--690. Stohr, P.E. and Goldring, S. Origin of somatosensory evoked scalp responses in man. J. Neurosurg., 1969, 31: 117--127,
65 Tsumoto, T., Hirose, N., Nonaka, S. and Takahashi, M. Cerebrovascular disease: changes in somatosensory evoked potentials associated with unilateral lesions. Electroenceph. clin. Neurophysiol., 1973, 35: 463--473. Velasco, M. and Velasco, F. Differential effect of task relevance on early and late components of cortical and subcortical somatic evoked potentials in man. Eiectroenceph. clin. Neurophysiol., 1975, 39: 353--364. Von Monakow, C. Die Lokalisation in Grosshirn und der Abbau der Funktion durch kortikale Herde. Bergmann, Wiesbaden, 1914: 26--34. Williamson, P.D., Golf, W.R. and Allison, T. Somatosensory evoked responses in patients with unilateral cerebral lesions. Electroenceph. clin. Neurophysiol., 1970, 20: 566--575. Yamada, T., McKee, J. and Kimura, J. The effect of peripheral ischemia on somatosensory evoked potentials. Electroenceph. clin. Neurophysiol., 1977, 43: 505. Yamada, T., Kimura, J., Young, S. and Powers, M. Somatosensory evoked potentials elicited by bilateral stimulation of the medial nerve and its clinical application. Neurology (Minneap.), 1978, 28: 218--223.
59
© Elsevier/North-Holland Scientific Publishers, Ltd.
S O M A T O S E N S O R Y E V O K E D POTENTIALS: A B N O R M A L I T I E S WITH FOCAL BRAIN LESIONS REMOTE F R O M THE P R I M A R Y S E N S O R I M O T O R A R E A 1 J.A. OBESO, J.F. MARTI-MASSO and N. CARRERA Division of Neurology, Residencia Sanitaria Nuestra Sra. de Aranzazu, San Sebastian (Spain)
(Accepted for publication: September 13, 1979) The clinical applications of somatosensory evoked potentials (SEPs) by means of an averaging technique have been extensively reported (Halliday 1967; Laget et al. 1967; Williamson et al. 1970; Desmedt and Noel 1973; Cracco 1975). Most previous studies have associated clinical impairment of joint position sensitivity with the appearance of SEP abnormalities (Halliday and Wakefield 1963; Giblin 1964; Noel and Desmedt 1975). Thus the integrity of both the dorsal columnmedial lemniscus pathway and primary sensorimotor area (PSMA) has been considered an essential requirement to record a normal SEP (Domino et al. 1965; Stohr and Goldring 1969). On the contrary, isolated lesions of the dorso-lateral ascending pathways or those placed away from the PSMA did n o t modify SEP characteristics (Bergamini and Bergamasco 1967; Halliday 1967; Noel and Desm e d t 1975). However, there are suggestions that SEPs contain several components arising from different neuronal sources, the early short latency potentials corresponding to the lemniscus-mediated responses and the late waves to the diffuse spino-thalamic projections (Abrahamian et al. 1963; Shagass and Schwartz 1964; Lewis 1970; Yamada et al. 1977). Recent investigations have shown altered SEPs in patients w i t h o u t sensory disturbances (Okasaki et al. 1971; Shibasaki et al. 1977; Yamada et al. 1978), giving a new dimension to the role of SEPs in assessing
brain activity under pathological conditions. The present work analyses the influence on SEPs of focal brain lesions placed remote from the PSMA, using the high accuracy of computerized tomography in detecting and localizing brain lesions (Ambrose et al. 1975; Jabobs et al. 1976).
Methods and materials Subjects
A total of 41 patients with supratentorial focal brain lesions was studied, 14 cases of brain t u m o r and 27 of cerebrovascular accident (Table I). Their ages ranged between 22 and 72 years. An equal number of normal volunteers served as controls. The site of the pathological lesion was determined in all cases by computerized tomography (CT). Clinical examination was performed by at least two neurologists on different days. Special care was taken to avoid the influence of acute changes in the clinical situation; thus no patient with cerebrovascular accident (CVA) was explored during the acute phase of the illness (first 2 weeks). To facilitate statistical analysis, subjects were arranged in 3 groups: group I, patients with lesions of the PSMA; group II, patients with lesions remote from the PSMA; and group III, normal volunteers (Table I). Clinical data
i Presented in part at the International Evoked Potentials Symposium, Nottingham (U.K.), 1978.
Sensory impairment as judged clinically was present in all patients of group I. 80% had
60
sensory deficits for all modalities, 11% presented mainly pain and temperature loss, and 18% showed visual agnosia, anosognosia and asomatognosia. In group II, 5 patients (24%) were f o u n d to have sensory defects, 3 were cases of tactile extinction and 2 of agraphaesthesia.
Recording procedure A Medelec electrophysiological system was used. SEPs were recorded in a dimly lit shielded room with the subject in a supine position with the eyes closed. The median nerve was electrically stimulated at the wrist, using a pair of surface electrodes placed 3 cm apart. Pulse duration was 0.1 msec. The stimulus intensity was adjusted to 10% above the m o t o r threshold of the opponens pollicis muscle in each case. Stimuli were delivered at intervals of 1--2 sec. Insulated stainless steel needles with a bared tip of 5 m m were used for recording both EEGs and SEPs. To record the SEPs, the active electrode was placed on C3 or C4 (10-20 system), and the reference electrode on Fz. The amplifier bandpass was 10--2000 c/sec (--3 dB), and the outputs were s u m m a t e d by a computer (Plurimat-S). Polaroid films were used to make permanent records of all potentials. One set of tests consisted of 256 averaged responses with an analysis time of 200 msec. Latencies were measured from the stimulus to each peak with a resolution of 0.2 msec. Amplitudes were defined as the heights of successive positivenegative peaks. Two-way analysis of variance and ×2 test were used for statistical analysis.
J.A. O B E S O E T AL.
]5"
flTO 10 S 0 5
+%%
p.
%,~
10
(÷)
50
150
IO0
did n o t reach statistical significance ( P > 0.05).
Relationship o f SEP abnormalities to the site and aetiology o f the lesion SEP abnormalities were f o u n d on the same side as the lesion in 20 out of 21 patients from group I (90%) and in 15 patients (71%) from group II. Over the intact hemisphere SEPs were altered in 9 cases (43%) from group I, and in 3 patients (15%) from group II (Table I). The aetiology of the lesion was not a significant factor for the incidence of abnormalities in either group (×2 test, P > 0.05). TABLE I SEP a b n o r m a l i t i e s a n d sites o f t h e lesions a c c o r d i n g t o aetiology. Localization
Results
Tumours
CVA *
Control group (III) SEP values for this group were similar to those reported by other authors (Giblin 1964; Desmedt and Noel 1973; Shibasaki et al. 1977; Yamada et al. 1978). In Fig. 1 a schematic SEP is the model of normality considered in this work. Variability between hemispheres, both individual and within the group,
200
Fig. 1. S c h e m a t i c SEP b y m e d i a n n e r v e s t i m u l a t i o n , w h i c h r e p r e s e n t s t h e average o f 40 n o r m a l v o l u n t e e r s . Positive waves are d o w n w a r d , b y c o n v e n t i o n in this a n d s u b s e q u e n t figures. T i m e in msec, a m p l i t u d e in mV.
A b n o r m a l SEP Affected side
Intact side
Group I PSMA
4
17
19
9
7 1 2
4 5 1
10 3 2
2 0 1
Group H Frontal Occipital Temporal
* CVA = cerebrovascular accident.
SEP ABNORMALITIES WITH FOCAL BRAIN LESIONS
61
TABLE II SEP abnormalities in patients with focal brain lesions. J~, increased latency;-~, decreased amplitude; t, increased duration; t t , increased amplitude. Affected hemisphere
Intact hemisphere
N-22
N-39
N-70
N-22
N-39
N-70
~t
19 17 5 0
18 11 14 0
12 6 3 0
4 2 8 7
3 6 5 5
0 3 3 2
5
2
2
0
0
0
t t~
4 10 16
4 15 14
4 7 9
0 2 2
0 1 2
0 0 0
G r o u p I (n = 21)
Group II (n = 20)
Relationship o f clinical data to SEP alterations When e v e r y i s o l a t e d p a r a m e t e r o f SEP was a n a l y s e d (Table II), i n c r e a s e d l a t e n c y a n d d e p r e s s e d a m p l i t u d e o f t h e first t w o waves (N-22 a n d N - 3 9 ) c o r r e l a t e d significantly w i t h lesions o f t h e P S M A a n d w i t h s e n s o r y deficits, while r e m o t e lesions a p p e a r e d t o be assoc i a t e d with i n c r e a s e d a m p l i t u d e o f N-22 a n d N - 3 9 (×: test, P < 0.01). T h e i n c i d e n c e o f SEP a n o m a l i e s in t h e i n t a c t h e m i s p h e r e was g r e a t e r in g r o u p I t h a n in g r o u p I I (P < 0.01). N e v e r t h e l e s s , t h e c h a n g e s in m o r p h o l o g y in t h e s e cases were similar t o t h o s e seen w i t h r e m o t e lesions on t h e a f f e c t e d h e m i s p h e r e (Fig. 2, 3 a n d 4). A b n o r m a l i t i e s o f the N-70 w a v e were p r e s e n t e q u a l l y in t h e t w o g r o u p s (×2 test, P > 0.05).
EEG and SEP abnormalities
Fig. 2. Top: CT scan showing a large right hemisphere infarct. Bottom: SEP of the left hemisphere (upper) and of the right (lower). Note that SEP is almost absent on the affected side and also abnormal on the intact side.
A c o m p a r a t i v e analysis o f t h e discriminat o r y p o w e r s o f SEPs a n d E E G s f o r d e t e c t i n g b r a i n d y s f u n c t i o n s h o w e d a slight s u p e r i o r i t y o f SEPs in b o t h g r o u p s a n d o v e r b o t h h e m i s p h e r e s (Table I I I ) . T h e s e d i f f e r e n c e s were significant for group I on the intact hemisphere a n d f o r g r o u p I i on t h e a f f e c t e d side (P < 0.01).
62
J.A. OBESO ET AL.
Fig. 4. Top: CT scan of a patient with a left occipital haematoma. Bottom: abnormal SEP, waves N-22 and N-39, on the affected side (upper) and normal response on the intact hemisphere (lower).
Fig. 3. Top: extensive temporo-parietal infarction on the right and small frontal infarct on the left. Bottom: the SEP on the left (upper) represents a typical trace for patients with lesions remote from the PSMA; the early waves are increased in amplitude and period, while the SEP recorded on the right (lower) is almost absent.
a n d N-39 (Giblin 1 9 6 4 ; Liberson 1 9 6 6 ; Laget et al. 1 9 6 7 ; Halliday 1 9 6 7 ; T s u m o t o et al. 1 9 7 3 ; Shibasaki et al. 1 9 7 7 ; Y a m a d a et al. 1 9 7 8 ) . B o t h changes c o r r e l a t e d well with clinical s e n s o r y deficits, as in m a n y o t h e r r e p o r t s ( A l a j o u a n i n e et al. 1 9 5 8 ; Halliday a n d Wake-
TABLE III Comparison of SEP and EEG rates of abnormality. Discussion On c o n s i d e r i n g the r e l a t i o n s h i p b e t w e e n SEP a b n o r m a l i t i e s a n d lesions involving the PSMA, o u r s t u d y c o n f i r m s a n d f u r t h e r d o c u m e n t s previous findings r e p o r t i n g l o n g e r latencies and r e d u c t i o n in a m p l i t u d e o f N-22
Group I Group II
Affected hemisphere
Intact hemisphere
SEP
EEG
SEP
EEG
19 16
18 12
10 3
4 2
SEP ABNORMALITIES WITH FOCAL BRAIN LESIONS field 1963; Bergamini and Bergamasco 1967; Desmedt and Noel 1973). The high incidence of SEP abnormalities among patients with lesions placed far away from the PSMA represents the most important finding of this study. These anomalies reveal a brain dysfunction remote from the original lesion, since both clinical and experimental research have clearly shown that PSMA is the main source of the early SEP waves (Kelly et al. 1965; Velasco and Velasco 1975; Lukas and Siegel 1977; Goff et al. 1977; Iragui-Madoz and Wiederholt 1977). This concept is very close to Von Monakow's theory of diaschisis (1914), which was first invoked by Larson et al. (1966) to explain their finding of SEP abnormalities in the intact hemisphere of patients with unilateral lesions. Studies on brain glucose metabolism (Meyer et al. 1970), regional cerebral blood flow (Endo et al. 1977; Slater et al. 1977) and cortical electrophysiology (Kempinsky 1958) support Von Monakow's original theory. From a purely neurophysiological point of view, we may state that lesions destroying the PSMA elicit an increase in latency and a decrease in amplitude of c o m p o n e n t s N-22 and N-39, as shown in Figs. 2 and 3. On the other hand, the main changes f o u n d in group II are increased duration and amplitude of N-22 and N-39 (Figs. 3 and 4). The latter changes may be interpreted as due to neuronal hypersynchronism secondary to metabolic alterations of PSMA neurones (Creutzfeldt and Houchin 1974), although direct evidence is n o t available yet. Changes of N-70 and later waves did n o t prove to be specific in our patients as was previously recognized by other authors (Shibasaki et al. 1977; Yamada et al. 1978). The N-70 wave seems to be subject to reticular influences and, thus, to reflect more closely the functional state of the reticulocortical pathways (Lukas and Siegel 1977). As a whole, SEPs are only slightly superior to the EEG in their ability to detect abnormalities. However, SEPs are of considerably greater value in localizing brain dysfunction, in agreem e n t with earlier publications (Mijoshi et al.
63 1971; Shibasaki et al. 1977). Present results allow the use of SEPs as a functional test to evaluate patients with cerebral lesions of any origin. Moreover, these findings may be a starting point to study the cortical mechanism involved in the recovery of certain brain functions after focal lesions, a matter of practical and theoretical interest.
Summary Somatosensory evoked potentials (SEPs) were recorded in 41 patients with focal brain lesions recognized by computerized tomography. 21 patients presented damage of the primary sensorimotor area (PSMA), and their SEPs were reduced in amplitude and increased in latency for the t w o early components (N-22 and N-39), in accordance with previous evidence. The other 20 patients presented lesions remote from the PSMA, 15 (71%) showing abnormal SEPs mainly c'haracterized by increment in amplitude and duration of N-22 and N-39. Abnormalities of the N-70 and later waves were n o t specific for any type of lesion. SEPs appeared more sensitive than the EEG for detecting brain dysfunction. The physiopathological and clinical importance of these findings are discussed.
Rdsumd Potentiels dvoquds somesthdsiques: anomalies rdsultant de ldsions focales du cortex sensorimoteur Les potentiels ~voqu~s somesth~siques (PES) ont dtd etudids chez 41 malades atteints de ldsions c~r~brales focales confirmdes par tomodensitomdtrie (TAC). Une ldsion du cortex sensorimoteur primaire (CSMP) a ~t~ d~celde chez 21 malades; leurs PES dtaient caractdrisds par une augmentation de la latence et une diminution de l'amplitude des premieres composantes (N-22, N-39). Les 20 autres malades, porteurs d'altdrations dioign~es du
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